Dataset Information

Polar vacuolar distribution is essential for accurate asymmetric division of Arabidopsis zygotes.

ABSTRACT: In most flowering plants, the asymmetric cell division of the zygote is the initial step in establishing the apical-basal axis of the mature plant. The zygote is polarized, possessing the nucleus at the apical tip and large vacuoles at the basal end. Despite their known polar localization, whether the positioning of the vacuoles and the nucleus is coordinated and what the role of the vacuole is in the asymmetric zygotic division remain elusive. In the present study, we utilized a live-cell imaging system to visualize the dynamics of vacuoles during the entire process of zygote polarization in Arabidopsis Image analysis revealed that the vacuoles formed tubular strands around the apically migrating nucleus. They gradually accumulated at the basal region and filled the space, resulting in asymmetric distribution in the mature zygote. To assess the role of vacuoles in the zygote, we screened various vacuole mutants and identified that shoot gravitropism2 (sgr2), in which the vacuolar structural change was impaired, failed to form tubular vacuoles and to polarly distribute the vacuole. In sgr2, large vacuoles occupied the apical tip and thus nuclear migration was blocked, resulting in a more symmetric zygotic division. We further observed that tubular vacuole formation and asymmetric vacuolar distribution both depended on the longitudinal array of actin filaments. Overall, our results show that vacuolar dynamics is crucial not only for the polar distribution along actin filaments but also for adequate nuclear positioning, and consequently zygote-division asymmetry.

SUBMITTER: Kimata Y

PROVIDER: S-EPMC6369786 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Polar vacuolar distribution is essential for accurate asymmetric division of <i>Arabidopsis</i> zygotes.

Kimata Yusuke Y Kato Takehide T Higaki Takumi T Kurihara Daisuke D Yamada Tomomi T Segami Shoji S Morita Miyo Terao MT Maeshima Masayoshi M Hasezawa Seiichiro S Higashiyama Tetsuya T Tasaka Masao M Ueda Minako M

Proceedings of the National Academy of Sciences of the United States of America 20190116 6

In most flowering plants, the asymmetric cell division of the zygote is the initial step in establishing the apical-basal axis of the mature plant. The zygote is polarized, possessing the nucleus at the apical tip and large vacuoles at the basal end. Despite their known polar localization, whether the positioning of the vacuoles and the nucleus is coordinated and what the role of the vacuole is in the asymmetric zygotic division remain elusive. In the present study, we utilized a live-cell imagi ...[more]

PMID: 30651313

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Project description:Although asymmetric deposition of the plant extracellular matrix is critical for the normal functioning of many cell types, the molecular mechanisms establishing this asymmetry are not well understood. During differentiation, Arabidopsis seed coat epidermal cells deposit large amounts of pectin-rich mucilage asymmetrically to form an extracellular pocket between the plasma membrane and the outer tangential primary cell wall. At maturity, the mucilage expands on contact with water, ruptures the primary cell wall, and extrudes to encapsulate the seed. In addition to polysaccharides, mucilage contains secreted proteins including the β-galactosidase MUCILAGE MODIFIED 2 (MUM2). A functional chimeric protein where MUM2 was fused translationally with Citrine yellow fluorescent protein (Citrine) indicated that MUM2-Citrine fluorescence preferentially accumulates in the mucilage pocket concomitant with mucilage deposition and rapidly disappears when mucilage synthesis ceases. A secreted form of Citrine, secCitrine, showed a similar pattern of localization when expressed in developing seed coat epidermal cells. This result suggested that both the asymmetric localization and rapid decrease of fluorescence is not unique to MUM2-Citrine and may represent the default pathway for secreted proteins in this cell type. v-SNARE proteins were localized only in the membrane adjacent to the mucilage pocket, supporting the hypothesis that the cellular secretory apparatus is redirected and targets secretion to the outer periclinal apoplast during mucilage synthesis. In addition, mutation of ECHIDNA, a gene encoding a TGN-localized protein involved in vesicle targeting, causes misdirection of mucilage, MUM2 and v-SNARE proteins from the apoplast/plasma membrane to the vacuole/tonoplast. Western blot analyses suggested that the disappearance of MUM2-Citrine fluorescence at the end of mucilage synthesis is due to protein degradation and because several proteases have been identified in extruded seed mucilage. However, as mutation of these genes did not result in a substantial delay in MUM2-Citrine degradation and the timing of their expression and/or their intracellular localization were not consistent with a role in MUM2-Citrine disappearance, the mechanism underlying the abrupt decrease of MUM2-Citrine remains unclear.

Dataset Information

Polar vacuolar distribution is essential for accurate asymmetric division of Arabidopsis zygotes.

Publications

Polar vacuolar distribution is essential for accurate asymmetric division of <i>Arabidopsis</i> zygotes.

Similar Datasets

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